Unlocking the binding and reaction mechanism of hydroxyurea substrates as biological nitric oxide donors

Journal of Chemical Information and Modeling

Volumn 52, Issue 5, 2012, Pages 1288-1297

  Vankayala, Sai Lakshmana ^a   Hargis, Jacqueline C ^a   Woodcock, H Lee ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAGNOSIS; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEMOGLOBIN; HYDROGEN BONDS; NITRIC OXIDE; PARAMAGNETIC RESONANCE; SUBSTRATES;

ELECTRON PARAMAGNETIC RESONANCES (EPR); ENERGETIC ANALYSIS; INTERACTION ENERGIES; NITRIC OXIDE DONOR; PRIMARY MECHANISM; REACTION MECHANISM; SICKLE CELL DISEASE; VIRTUAL SCREENING;

BINDING ENERGY;

HEMOGLOBIN; HYDROXYUREA; LIGAND; NITRIC OXIDE DONOR;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DRUG EFFECT; ENZYME SPECIFICITY; HUMAN; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; HEMOGLOBINS; HUMANS; HYDROXYUREA; LIGANDS; MODELS, MOLECULAR; NITRIC OXIDE DONORS; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 84861504711     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300035c     Document Type: Article

References (70)

1. Sutton, M.; Atweh, G. F.; Cashman, T. D.; Davis, W. T. Resolving conflicts: misconceptions and myths in the care of the patient with sickle cell disease Mt. Sinai J. Med. 1999, 66, 282-285
2. Kotiah, S. D.; Ballas, S. K. Investigational drugs in sickle cell anemia Expert Opin. Invest. Drugs 2009, 18, 1817-1828
3. Frenette, P. S.; Atweh, G. F. Sickle cell disease: old discoveries, new concepts, and future promise J. Clin. Invest. 2007, 117, 850-858 (Pubitemid 46556737)
4. Colombatti, R.; Maschietto, N.; Varotto, E.; Grison, A.; Grazzina, N.; Meneghello, L.; Teso, S.; Carli, M.; Milanesi, O.; Sainati, L. Pulmonary hypertension in sickle cell disease children under 10 years of age Br. J. Hamaetol. 2010, 150, 601-609
5. de Franceschi, L.; Finco, G.; Vassanelli, A.; Zaia, B.; Ischia, S.; Corrocher, R. A pilot study on the efficacy of ketorolac plus tramadol infusion combined with erythrocytapheresis in the management of acute severe vaso-occlusive crises and sickle cell pain Haematologica 2004, 89, 1389-1391 (Pubitemid 39540576)
6. Tang, D. C.; Prauner, R.; Liu, W.; Kim, K.-H.; Hirsch, R. P.; Driscoll, M. C.; Rodgers, G. P. Polymorphisms within the angiotensinogen gene (GT-repeat) and the risk of stroke in pediatric patients with sickle cell disease: A case-control study Am. J. Hematol. 2001, 68, 164-169 (Pubitemid 32983204)
7. Olowoyeye, A.; Okwundu Charles, I. Gene therapy for sickle cell disease Cochrane Database Syst. Rev. 2010, CD007652
8. Steinberg, M. H.; Brugnara, C. Pathophysiological-based approaches to treatment of sickle cell disease Annu. Rev. Med. 2003, 54, 89-112 (Pubitemid 37390845)
9. Lou, T.-F.; Singh, M.; Mackie, A.; Li, W.; Pace Betty, S. Hydroxyurea generates nitric oxide in human erythroid cells: mechanisms for gamma-globin gene activation Exp. Biol. Med. (Maywood) 2009, 234, 1374-1382
10. Watson, J.; Stahman, A. W.; Bilello, F. P. The significance of the paucity of sickle cells in newborn negro infants Am. J. Med. Sci. 1948, 215, 419-423
11. Noble, A., The respiratory system. In A foundation for neonatal care: a multi-disciplinary guide, 1 ed.; Hall, M.; N., A.; Smith, S., Ed.; Radcliffe Medical PR: Abingdon, Oxon, OX 1AA, U.K., 2009; pp 158-160.
12. Charache, S.; Terrin, M. L.; Moore, R. D.; Dover, G. J.; Barton, F. B.; Eckert, S. V.; McMahon, R. P.; Bonds, D. R. Effect of hydroxyurea on the frequency of painful crises in sickle cell anemia. Investigators of the Multicenter Study of Hydroxyurea in Sickle Cell Anemia N. Engl. J. Med. 1995, 332, 1317-1322
13. Weiner, D. L.; Hibberd, P. L.; Betit, P.; Copper, A. B.; Botelho, C. A.; Brugunara, C. Preliminary assessment of inhaled nitric oxide for acute vaso-occlusive crisis in pediatric patients with sickle cell disease JAMA, J. Am. Med. Assoc. 2003, 289, 1136-1142 (Pubitemid 37430328)
14. Cokic, V. P.; Smith, R. D.; Beleslin-Cokic, B. B.; Njoroge, J. M.; Miller, J. L.; Gladwin, M. T.; Schechter, A. N. Hydroxyurea induces fetal hemoglobin by the nitric oxide-dependent activation of soluble guanylyl cyclase J. Clin. Invest. 2003, 111, 231-239 (Pubitemid 36105922)
15. Singh, H.; Dulhani, N.; Kumar, B. N.; Singh, P.; Tiwari, P. Effective control of sickle cell disease with hydroxyurea therapy Ind. J. Pharmacol. 2010, 42, 32-35
16. King, S. B. The nitric oxide producing reactions of hydroxyurea Curr. Med. Chem. 2003, 10, 437-452 (Pubitemid 36221573)
17. Huang, J.; Zou, Z.; Kim-Shapiro, D. B.; Ballas, S. K.; King, S. B. Hydroxyurea Analogues As Kinetic and Mechanistic Probes of the Nitric Oxide Producing Reactions of Hydroxyurea and Oxyhemoglobin J. Med. Chem. 2003, 46, 3748-3753 (Pubitemid 36988660)
18. Rohrman, B. A.; Mazziotti, D. A. Quantum Chemical Design of Hydroxyurea Derivatives for the Treatment of Sickle-Cell Anemia J. Phys. Chem. B 2005, 109, 13392-13396 (Pubitemid 41048749)
19. King, S. B. N-hydroxyurea and acyl nitroso compounds as nitroxyl (HNO) and nitric oxide (NO) donors Curr. Top. Med. Chem. (Sharjah, United Arab Emirates) 2005, 5, 665-673 (Pubitemid 41179726)
20. Lepeshkevich, S. V.; Parkhats, M. V.; Stepuro, I. I.; Dzhagarov, B. M. Molecular oxygen binding with α and β subunits within the R quaternary state of human hemoglobin in solutions and porous sol-gel matrices Biochim. Biophys. Acta, Proteins Proteomics 2009, 1794, 1823-1830
21. Safo, M. K.; Ahmed, M. H.; Ghatge, M. S.; Boyiri, T. Hemoglobin-ligand binding: Understanding Hb function and allostery on atomic level Biochim. Biophys. Acta, Proteins Proteomics 2011, 1814, 797-809
22. Park, S.-Y.; Yokoyama, T.; Shibayama, N.; Shiro, Y.; Tame, J. R. H. 1.25 Å resolution crystal structures of human hemoglobin in the oxy, deoxy and carbonmonoxy forms J. Mol. Biol. 2006, 360, 690-701 (Pubitemid 43977865)
23. Yuan, Y.; Simplaceanu, V.; Ho, N. T.; Ho, C. An Investigation of the Distal Histidyl Hydrogen Bonds in Oxyhemoglobin: Effects of Temperature, pH, and Inositol Hexaphosphate Biochemistry 2010, 49, 10606-10615
24. Kanias, T.; Acker, J. P. Biopreservation of red blood cells-the struggle with hemoglobin oxidation Febs J. 2010, 277, 343-356
25. Bellelli, A. Hemoglobin and cooperativity: experiments and theories Curr. Protein Pept. Sci. 2010, 11, 2-36
26. Yonetani, T.; Laberge, M. Protein dynamics explain the allosteric behaviors of hemoglobin Biochim. Biophys. Acta, Proteins Proteomics 2008, 1784, 1146-1158
27. Dzhagarov, B. M.; Lepeshkevich, S. V. Kinetic studies of differences between α- and β-chains of human hemoglobin: an approach for determination of the chain affinity to oxygen Chem. Phys. Lett. 2004, 390, 59-64
28. Umbreit, J. Methemoglobin-it's not just blue: a concise review Am. J. Hematol. 2007, 82, 134-144 (Pubitemid 46155276)
29. King, S. B. C-Nitroso compounds, oximes, N-hydroxyguanidines and N-hydroxyureas Nitric Oxide Donors 2005, 177-199
30. Huang, J.; Hadimani, S. B.; Rupon, J. W.; Ballas, S. K.; Kim-Shapiro, D. B.; King, S. B. Iron Nitrosyl Hemoglobin Formation from the Reactions of Hemoglobin and Hydroxyurea Biochemistry 2002, 41, 2466-2474 (Pubitemid 34160911)
31. Pacelli, R.; Taira, J.; Cook, J. A.; Wink, D. A.; Krishna, M. C. Hydroxyurea reacts with heme proteins to generate nitric oxide Lancet 1996, 347, 900 (Pubitemid 26099551)
32. Sherman, W.; Beard, H. S.; Farid, R. Use of an induced fit receptor structure in virtual screening Chem. Biol. Drug Des. 2006, 67, 83-84 (Pubitemid 43881391)
33. Sherman, W.; Day, T.; Jacobson, M. P.; Friesner, R. A.; Farid, R. Novel Procedure for Modeling Ligand/Receptor Induced Fit Effects J. Med. Chem. 2006, 49, 534-553 (Pubitemid 43157487)
34. Konc, J.; Cesnik, T.; Konc, J. T.; Penca, M.; Janezic, D. ProBiS-Database: Precalculated Binding Site Similarities and Local Pairwise Alignments of PDB Structures J. Chem. Inf. Model. 2012, 52, 604-612
35. Konc, J.; Janezic, D. ProBiS algorithm for detection of structurally similar protein binding sites by local structural alignment Bioinformatics 2010, 26, 1160-1168
36. Konc, J.; Janezic, D. ProBiS: a web server for detection of structurally similar protein binding sites Nucleic Acids Res. 2010, 38, W436-W440
37. Larkin, M. A.; Blackshields, G.; Brown, N. P.; Chenna, R.; McGettigan, P. A.; McWilliam, H.; Valentin, F.; Wallace, I. M.; Wilm, A.; Lopez, R.; Thompson, J. D.; Gibson, T. J.; Higgins, D. G. Clustal W and Clustal X version 2.0 Bioinformatics 2007, 23, 2947-2948 (Pubitemid 350162903)
38. Chen, H.; Ikeda-Saito, M.; Shaik, S. Nature of the Fe-O2 Bonding in Oxy-Myoglobin: Effect of the Protein J. Am. Chem. Soc. 2008, 130, 14778-14790
39. Park, S.-Y.; Yokoyama, T.; Shibayama, N.; Shiro, Y.; Tame Jeremy, R. H. 1.25 A resolution crystal structures of human haemoglobin in the oxy, deoxy and carbonmonoxy forms J. Mol. Biol. 2006, 360, 690-701 (Pubitemid 43977865)
40. Dodson, E.; Dodson, G. Movements at the hemoglobin A-hemes and their role in ligand binding, analyzed by X-ray crystallography Biopolymers 2009, 91, 1056-1063
41. De Rosa, M. C.; Alinovi, C. C.; Russo, A.; Giardina, B. Binding modes of L35 to α- and β-semihemoglobins: Structural insights into the inequivalence of α- and β-subunits of hemoglobin Biochem. Biophys. Res. Commun. 2007, 354, 720-726 (Pubitemid 46186244)
42. Marechal, J.-D.; Maseras, F.; Lledos, A.; Mouawad, L.; Perahia, D. A DFT study on the relative affinity for oxygen of the α and β subunits of hemoglobin J. Comput. Chem. 2006, 27, 1446-1453 (Pubitemid 44230431)
43. Birukou, I.; Schweers, R. L.; Olson, J. S. Distal Histidine Stabilizes Bound O2 and Acts as a Gate for Ligand Entry in Both Subunits of Adult Human Hemoglobin J. Biol. Chem. 2010, 285, 8840-8854
44. Lukin, J. A.; Simplaceanu, V.; Zou, M.; Ho, N. T.; Ho, C. NMR reveals hydrogen bonds between oxygen and distal histidines in oxyhemoglobin Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 10354-10358
45. Suzuki, T.; Watanabe, Y.-H.; Nagasawa, M.; Matsuoka, A.; Shikama, K. Dual nature of the distal histidine residue in the autoxidation reaction of myoglobin and hemoglobin. Comparison of the H64 mutants Eur. J. Biochem. 2000, 267, 6166-6174
46. Friesner, R. A.; Murphy, R. B.; Repasky, M. P.; Frye, L. L.; Greenwood, J. R.; Halgren, T. A.; Sanschagrin, P. C.; Mainz, D. T. Extra Precision Glide: Docking and Scoring Incorporating a Model of Hydrophobic Enclosure for Protein-Ligand Complexes J. Med. Chem. 2006, 49, 6177-6196 (Pubitemid 44595196)
47. Jacobson, M. P.; Friesner, R. A.; Xiang, Z.; Honig, B. On the Role of the Crystal Environment in Determining Protein Side-chain Conformations J. Mol. Biol. 2002, 320, 597-608 (Pubitemid 34753983)
48. Jacobson, M. P.; Pincus, D. L.; Rapp, C. S.; Day, T. J. F.; Honig, B.; Shaw, D. E.; Friesner, R. A. A hierarchical approach to all-atom protein loop prediction Proteins Struct., Funct., Bioinf. 2004, 55, 351-367 (Pubitemid 38437493)
49. Agostino, M.; Jene, C.; Boyle, T.; Ramsland, P. A.; Yuriev, E. Molecular Docking of Carbohydrate Ligands to Antibodies: Structural Validation against Crystal Structures J. Chem. Inf. Model. 2009, 49, 2749-2760
50. Jorgensen, W. L.; Maxwell, D. S.; Tirado-Rives, J. Development and Testing of the OPLS All-Atom Force Field on Conformational Energetics and Properties of Organic Liquids J. Am. Chem. Soc. 1996, 118, 11225-11236 (Pubitemid 26399746)
51. Vanommeslaeghe, K.; Hatcher, E.; Acharya, C.; Kundu, S.; Zhong, S.; Shim, J.; Darian, E.; Guvench, O.; Lopes, P.; Vorobyov, I.; Mackerell, A. D., Jr. CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields J. Comput. Chem. 2010, 31, 671-690
52. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and testing of a general Amber force field J. Comput. Chem. 2004, 25, 1157-1174
53. Kolossvary, I.; Guida, W. C. Low-mode conformational search elucidated: application to C39H80 and flexible docking of 9-deazaguanine inhibitors into PNP J. Comput. Chem. 1999, 20, 1671-1684 (Pubitemid 129653223)
54. Gadakar, P. K.; Phukan, S.; Dattatreya, P.; Balaji, V. N. Pose Prediction Accuracy in Docking Studies and Enrichment of Actives in the Active Site of GSK-3β J. Chem. Inf. Model. 2007, 47, 1446-1459 (Pubitemid 47210048)
55. Celik, L.; Sinning, S.; Severinsen, K.; Hansen, C. G.; Moller, M. S.; Bols, M.; Wiborg, O.; Schiott, B. Binding of Serotonin to the Human Serotonin Transporter. Molecular Modeling and Experimental Validation J. Am. Chem. Soc. 2008, 130, 3853-3865 (Pubitemid 351429851)
56. Liao, C.; Park, J.-E.; Bang, J. K.; Nicklaus, M. C.; Lee, K. S. Probing Binding Modes of Small Molecule Inhibitors to the Polo-Box Domain of Human Polo-like Kinase 1 ACS Med. Chem. Lett. 2010, 1, 110-114
57. Felts, A. K.; LaBarge, K.; Bauman, J. D.; Patel, D. V.; Himmel, D. M.; Arnold, E.; Parniak, M. A.; Levy, R. M. Identification of Alternative Binding Sites for Inhibitors of HIV-1 Ribonuclease H Through Comparative Analysis of Virtual Enrichment Studies J. Chem. Inf. Model. 2011, 51, 1986-1998
58. Babaoglu, K.; Shoichet, B. K. Deconstructing fragment-based inhibitor discovery Nat. Chem. Biol. 2006, 2, 720-723 (Pubitemid 44764214)
59. McRobb, F. M.; Capuano, B.; Crosby, I. T.; Chalmers, D. K.; Yuriev, E. Homology Modeling and Docking Evaluation of Aminergic G Protein-Coupled Receptors J. Chem. Inf. Model. 2010, 50, 626-637
60. Barreca, M. L.; Iraci, N.; De Luca, L.; Chimirri, A. Induced-Fit Docking Approach Provides Insight into the Binding Mode and Mechanism of Action of HIV-1 Integrase Inhibitors ChemMedChem 2009, 4, 1446-1456
61. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations J. Comput. Chem. 1983, 4, 187-217
62. Miller, B. T.; Singh, R. P.; Klauda, J. B.; Hodoscek, M.; Brooks, B. R.; Woodcock, H. L., III CHARMMing: A New, Flexible Web Portal for CHARMM J. Chem. Inf. Model. 2008, 48, 1920-1929
63. Brooks, B. R.; Brooks, C. L., III; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S.; Caflisch, A.; Caves, L.; Cui, Q.; Dinner, A. R.; Feig, M.; Fischer, S.; Gao, J.; Hodoscek, M.; Im, W.; Kuczera, K.; Lazaridis, T.; Ma, J.; Ovchinnikov, V.; Paci, E.; Pastor, R. W.; Post, C. B.; Pu, J. Z.; Schaefer, M.; Tidor, B.; Venable, R. M.; Woodcock, H. L.; Wu, X.; Yang, W.; York, D. M.; Karplus, M. CHARMM: The biomolecular simulation program J. Comput. Chem. 2009, 30, 1545-1614
64. Misra, H. P.; Fridovich, I. Generation of superoxide radical during the autoxidation of hemoglobin J. Biol. Chem. 1972, 247, 6960-6962
65. Konc, J. J., D. An Improved Branch and Bound Algorithm for the Maximum Clique Problem MATCH Commun Math. Comput. Chem. 2007, 58, 569-590
66. Simonneaux, G.; Bondon, A. Mechanism of electron transfer in heme proteins and models: The NMR approach Chem. Rev. 2005, 105, 2627-2646 (Pubitemid 40951787)
67. Kiger, L.; Marden, M. C. Electron transfer kinetics between hemoglobin subunits J. Biol. Chem. 2001, 276, 47937-47943
68. Li, C.-z.; Liu, G.; Prabhulkar, S. Comparison of kinetics of hemoglobin electron transfer in solution and immobilized on electrode surface Am. J. Biomed. Sci. 2009, 1, 283-294
69. Huang, J.; Kim-Shapiro, D. B.; King, S. B. Catalase-Mediated Nitric Oxide Formation from Hydroxyurea J. Med. Chem. 2004, 47, 3495-3501 (Pubitemid 38822011)
70. Juul, T.; Malolepszy, A.; Dybkaer, K.; Kidmose, R.; Rasmussen, J. T.; Andersen, G. R.; Johnsen, H. E.; Jorgensen, J.-E.; Andersen, S. U. The in Vivo Toxicity of Hydroxyurea Depends on Its Direct Target Catalase J. Biol. Chem. 2010, 285, 21411-21415